Abstract
Exosomes, small extracellular vesicles with diameters of 40-100nm, are generated through the fusion of multivessel with plasma membrane and secreted by a variety of living cells. Exosomes contain lipid bilayer membrane and releasable functionally active proteins, mRNA and microRNAs (miRNAs). This article reviews the latest progress of researches on exosomes in diseases that lead to infertility.
Keywords: Exosomes, reproductive medicine, endometriosis, polycystic ovary syndrome, infertility, diseases.
[1]
Barkalina N, Jones C, Wood MJA, Coward K. Extracellular vesicle-mediated delivery of molecular compounds into gametes and embryos: Learning from nature. Hum Reprod Update 2015; 21(5): 627-39.
[2]
Keller S, Sanderson MP, Stoeck A, Altevogt P. Exosomes: From biogenesis and secretion to biological function. Immunol Lett 2006; 107(2): 102-8.
[3]
Mathivanan S, Ji H, Simpson RJ. Exosomes: Extracellular organelles important in intercellular communication. J Proteomics 2010; 73(10): 1907-20.
[4]
Akers JC, Gonda D, Kim R, Carter BS, Chen CC. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol 2013; 113(1): 1-11.
[5]
Crescitelli R, Lasser C, Szabo TG, et al. Distinct RNA profiles in subpopulations of extracellular vesicles: Apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2013; 2.
[6]
Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 2000; 113(Pt 19): 3365-74.
[7]
Laulagnier K, Grand D, Dujardin A, et al. PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett 2004; 572(1-3): 11-4.
[8]
Di Pietro C. Exosome-mediated communication in the ovarian follicle. J Assist Reprod Genet 2016; 33(3): 303-11.
[9]
Halicka HD, Bedner E, Darzynkiewicz Z. Segregation of RNA and separate packaging of DNA and RNA in apoptotic bodies during apoptosis. Exp Cell Res 2000; 260(2): 248-56.
[10]
Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: Artefacts no more. Trends Cell Biol 2009; 19(2): 43-51.
[11]
Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30: 255-89.
[12]
Momen-Heravi F, Balaj L, Alian S, et al. Impact of biofluid viscosity on size and sedimentation efficiency of the isolated microvesicles. Front Physiol 2012; 3: 162.
[13]
Momen-Heravi F, Saha B, Kodys K, Catalano D, Satishchandran A, Szabo G. Increased number of circulating exosomes and their microRNA cargos are potential novel biomarkers in alcoholic hepatitis. J Transl Med 2015; 13: 261.
[14]
Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6): 654-9.
[15]
Kalluri R, LeBleu VS. Discovery of double-stranded genomic dna in circulating exosomes. Cold Spring Harb Symp Quant Biol 2016; 81: 275-80.
[16]
Wei Z, Batagov AO, Schinelli S, et al. Coding and noncoding landscape of extracellular RNA released by human glioma stem cells. Nat Commun 2017; 8(1): 1145.
[17]
Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011; 2: 180.
[18]
Skog J, Wurdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10(12): 1470-6.
[19]
da Silveira JC, de Avila A, Garrett HL, Bruemmer JE, Winger QA, Bouma GJ. Cell-secreted vesicles containing microRNAs as regulators of gamete maturation. J Endocrinol 2018; 236(1): R15-27.
[20]
Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122(6): 829-38.
[21]
Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: Oocytes carry the conversation. Science 2002; 296(5576): 2178-80.
[22]
da Silveira JC, Veeramachaneni DN, Winger QA, Carnevale EM, Bouma GJ. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol Reprod 2012; 86(3): 71.
[23]
Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006; 132(2): 191-206.
[24]
Boyer A, Goff AK, Boerboom D. WNT signaling in ovarian follicle biology and tumorigenesis. Trends Endocrinol Metab 2010; 21(1): 25-32.
[25]
Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol 2009; 7: 40.
[26]
Fortune JE. Ovarian follicular growth and development in mammals. Biol Reprod 1994; 50(2): 225-32.
[27]
Rodgers RJ, Irving-Rodgers HF. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod 2010; 82(6): 1021-9.
[28]
Al-Dossary AA, Strehler EE, Martin-Deleon PA. Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS One 2013; 8(11)e80181
[29]
Campoy I, Lanau L, Altadill T, et al. Exosome-like vesicles in uterine aspirates: a comparison of ultracentrifugation-based isolation protocols. J Transl Med 2016; 14(1): 180.
[30]
Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110(1): 13-21.
[31]
Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011; 108(12): 5003-8.
[32]
Bulun SE, Utsunomiya H, Lin Z, et al. Steroidogenic factor-1 and endometriosis. Mol Cell Endocrinol 2009; 300(1-2): 104-8.
[33]
Verkauf BS. Incidence, symptoms, and signs of endometriosis in fertile and infertile women. J Fla Med Assoc 1987; 74(9): 671-5.
[34]
Macer ML, Taylor HS. Endometriosis and infertility: A review of the pathogenesis and treatment of endometriosis-associated infertility. Obstet Gynecol Clin North Am 2012; 39(4): 535-49.
[36]
Fassbender A, Burney RO. F. O D, D’Hooghe T, Giudice L. Update on Biomarkers for the Detection of Endometriosis. BioMed Res Int 2015; 2015: 1-14.
[37]
Leone Roberti Maggiore U, Ferrero S, Mangili G, et al. A systematic review on endometriosis during pregnancy: Diagnosis, misdiagnosis, complications and outcomes. Hum Reprod Update 2016; 22(1): 70-103.
[38]
Nogales FF, Martin F, Linares J, Naranjo R, Concha A. Myxoid change in decidualized scar endometriosis mimicking malignancy. J Cutan Pathol 1993; 20(1): 87-91.
[39]
Gordts S, Puttemans P, Gordts S, Brosens I. Ovarian endometrioma in the adolescent: a plea for early-stage diagnosis and full surgical treatment. Gynecol Surg 2015; 12(1): 21-30.
[40]
Maged AM, Deeb WS, El Amir A, et al. Diagnostic accuracy of serum miR-122 and miR-199a in women with endometriosis. Int J Gynaecol Obstet 2018; 141(1): 14-9.
[41]
Wang WT, Zhao YN, Han BW, Hong SJ, Chen YQ. Circulating microRNAs identified in a genome-wide serum microRNA expression analysis as noninvasive biomarkers for endometriosis. J Clin Endocrinol Metab 2013; 98(1): 281-9.
[42]
Petracco R, Grechukhina O, Popkhadze S, Massasa E, Zhou Y, Taylor HS. MicroRNA 135 regulates HOXA10 expression in endometriosis. J Clin Endocrinol Metab 2011; 96(12): E1925-33.
[43]
Toloubeydokhti T, Pan Q, Luo X, Bukulmez O, Chegini N. The expression and ovarian steroid regulation of endometrial micro-RNAs. Reprod Sci 2008; 15(10): 993-1001.
[44]
Maas JW, Groothuis PG, Dunselman GA, de Goeij AF, Struyker Boudier HA, Evers JL. Endometrial angiogenesis throughout the human menstrual cycle. Hum Reprod 2001; 16(8): 1557-61.
[45]
Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulationAm J Pathol 1927; 3(2): 93-110 43
[46]
Rocha AL, Reis FM, Taylor RN. Angiogenesis and endometriosis. Obstet Gynecol Int 2013; 2013859619
[47]
Edwards AK, Nakamura DS, Virani S, Wessels JM, Tayade C. Animal models for anti-angiogenic therapy in endometriosis. J Reprod Immunol 2013; 97(1): 85-94.
[48]
Harp D, Driss A, Mehrabi S, et al. Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res 2016; 365(1): 187-96.
[49]
Mineo M, Garfield SH, Taverna S, Flugy A, De Leo G, Alessandro R, et al. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis 2012; 15(1): 33-45.
[50]
Paggetti J, Haderk F, Seiffert M, et al. Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 2015; 126(9): 1106-17.
[51]
Pascucci L, Alessandri G, Dall’Aglio C, et al. Membrane vesicles mediate pro-angiogenic activity of equine adipose-derived mesenchymal stromal cells. Vet J 2014; 202(2): 361-6.
[52]
Bao F, Wu P, Xiao N, Qiu F, Zeng QP. Nitric oxide-driven hypoxia initiates synovial angiogenesis, hyperplasia and inflammatory lesions in mice. PLoS One 2012; 7(3)e34494
[53]
Guduric-Fuchs J, O’Connor A, Cullen A, et al. Deep sequencing reveals predominant expression of miR-21 amongst the small non-coding RNAs in retinal microvascular endothelial cells. J Cell Biochem 2012; 113(6): 2098-111.
[54]
Xu Y, Luo F, Liu Y, et al. Exosomal miR-21 derived from arsenite-transformed human bronchial epithelial cells promotes cell proliferation associated with arsenite carcinogenesis. Arch Toxicol 2014; 89(7): 1071-82.
[55]
Norman RJ, Dewailly D, Legro RS, Hickey TE. Polycystic ovary syndrome. Lancet 2007; 370(9588): 685-97.
[56]
Patel S. Polycystic ovary syndrome (PCOS), an inflammatory, systemic, lifestyle endocrinopathy. J Steroid Biochem Mol Biol 2018; 182: 27-36.
[57]
Koiou E, Tziomalos K, Katsikis I, Papadakis E, Kandaraki EA, Panidis D. Platelet-derived microparticles in overweight/obese women with the polycystic ovary syndrome. Gynecol Endocrinol 2013; 29(3): 250-3.
[58]
Willis GR, Connolly K, Ladell K, et al. Young women with polycystic ovary syndrome have raised levels of circulating annexin V-positive platelet microparticles. Hum Reprod 2014; 29(12): 2756-63.
[59]
Kim YS, Kim MS, Lee SH, et al. Proteomic analysis of recurrent spontaneous abortion: Identification of an inadequately expressed set of proteins in human follicular fluid. Proteomics 2006; 6(11): 3445-54.
[60]
Berker B, Kaya C, Aytac R, Satiroglu H. Homocysteine concentrations in follicular fluid are associated with poor oocyte and embryo qualities in polycystic ovary syndrome patients undergoing assisted reproduction. Hum Reprod 2009; 24(9): 2293-302.
[61]
Wu YT, Tang L, Cai J, et al. High bone morphogenetic protein-15 level in follicular fluid is associated with high quality oocyte and subsequent embryonic development. Hum Reprod 2007; 22(6): 1526-31.
[62]
Yang Q, Liu LX, Huang HF. Extraction and identification of exosomes in follicular fluid from patients with polycystic ovary syndrome and isolation and detection of miRNAs in exosomes. J Shanghai Jiao Tong Uni(Med Sci) 2017; 37(8): 1085-9.
[63]
Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004; 116(2): 281-97.
[64]
Kloosterman WP, Plasterk RHA. The Diverse Functions of MicroRNAs in Animal Development and Disease. Dev Cell 2006; 11(4): 441-50.
[65]
Kuklina EV, Ayala C, Callaghan WM. Hypertensive disorders and severe obstetric morbidity in the United States. Obstet Gynecol 2009; 113(6): 1299-306.
[66]
Pillay P, Moodley K, Moodley J, Mackraj I. Placenta-derived exosomes: Potential biomarkers of preeclampsia. Int J Nanomedicine 2017; 12: 8009-23.
[67]
Dzhambov AM. Letter to the Editor on “Exposure to environmental noise and risk for male infertility: A 2population-based cohort study”. Environ Pollut 2017; 231(Pt 1): 1209-10.
[68]
Yang C, Guo WB, Zhang WS, et al. Comprehensive proteomics analysis of exosomes derived from human seminal plasma. Andrology 2017; 5(5): 1007-15.
[69]
Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 2009; 69(2): 159-67.
[70]
Wang C, Yang C, Chen X, et al. Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clin Chem 2011; 57(12): 1722-31.
[71]
Abu-Halima M, Ludwig N, Hart M, et al. Altered micro-ribonucleic acid expression profiles of extracellular microvesicles in the seminal plasma of patients with oligoasthenozoospermia Fertil Steril 2016; 106(5): 1061-9 e3
[72]
Vojtech L, Woo S, Hughes S, et al. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res 2014; 42(11): 7290-304.
[73]
Barcelo M, Mata A, Bassas L, Larriba S. Exosomal microRNAs in seminal plasma are markers of the origin of azoospermia and can predict the presence of sperm in testicular tissue. Hum Reprod 2018; 33(6): 1087-98.
[74]
Blazquez R, Sanchez-Margallo FM, Alvarez V, Uson A, Marinaro F, Casado JG. Fibrin glue mesh fixation combined with mesenchymal stem cells or exosomes modulates the inflammatory reaction in a murine model of incisional hernia. Acta Biomater 2018; 71: 318-29.
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